Ladybeetles (Coccinellidae)

Helen Roy, Alain Migeon

To cite this version:

Helen Roy, Alain Migeon. Ladybeetles (Coccinellidae). Alien terrestrial arthropods of Europe, 4 (1),
Pensoft Publishers, 2010, BioRisk, 978-954-642-554-6. �10.3897/biorisk.4.49�. �hal-02820802�

HAL Id: hal-02820802

https://hal.inrae.fr/hal-02820802
Submitted on 6 Jun 2020

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est

archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d’enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.
 A peer-reviewed open-access journal

BioRisk
BioRisk 4(1): 293–313 (2010)
Ladybeetles (Coccinellidae). Chapter 8.4 293
doi: 10.3897/biorisk.4.49 RESEARCH ARTICLE
www.pensoftonline.net/biorisk

Ladybeetles (Coccinellidae)
Chapter 8.4

Helen Roy1, Alain Migeon2

1 NERC Centre for Ecology & Hydrology, Biological Records Centre, Crowmarsh Gifford, Oxfordshire, OX10
8BB, United Kindgom 2 INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), Centre de Biologie et
Génétique des populations, CS 30016, 34988 Montferrier- sur-Lez Cedex, France

Corresponding authors: Helen Roy (hele@ceh.ac.uk), Alain Migeon (migeon@supagro.inra.fr)

Academic editor: Alain Roques    |    Received  26 January 2010    |    Accepted 22 May 2010    |    Published 6 July  2010

Citation: Roy H, Migeon A (2010) Ladybeetles (Coccinellidae). Chapter 8.4. In: Roques A et al. (Eds) Alien terrestrial
arthropods of Europe. BioRisk 4(1): 293–313. doi: 10.3897/biorisk.4.49

Abstract
The majority of Coccinellidae are beneficial predators and they have received considerable research atten-
tion because of their potential as biological control agents. Indeed the role of coccinellids as predators of
pest insects has been a major factor in the movement of coccinellids between countries. The commercial
production of coccinellids by biological control companies and local producers led to a rapid increase in
distribution thoughout the 1990’s. To date, 13 alien coccinellid species have been documented in Europe;
11 of these are alien to Europe (two are alien to Great Britain and Sweden but native within Europe).
The distribution of alien coccinellids in Europe mirrors the biogeographical distribution and patterns of
introduction. Some species have dispersed widely; Harmonia axyridis has spread rapidly from countries
where it was deliberately introduced to many others across Europe. The ecological and economic impacts
of alien coccinellids are not well documented. In this chapter we provide an overview of the temporal and
spatial patterns of alien coccinellids in Europe.

Keywords
Coccinellid, ladybird, alien, Europe, biological control agent, Harmonia axyridis, distribution patterns

8.4.1 Introduction
The Coccinellidae are commonly referred to as ladybirds (Britain, Australia, South
Africa), ladybugs (North America) or ladybeetles (various countries). Coccinellids
have received considerable research attention because of their role as predators of pest

Copyright H. Roy, A. Migeon. This is an open access article distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
294 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

insects. The Coccinellidae comprises over 4200 species worldwide (Iperti 1999, Ma-
jerus et al. (2006a)). Audisio and Canepari 2009 report that there are approximately
253 species and subspecies of Coccinellid in Europe. However, a review in 1999
documented only 110 species including species acclimatized through the 1900s: Ro-
dolia cardinalis, Cryptolaemus montrouzieri, Rhyzobius (Lindorus) lophanthae, Rhyzo-
bius forestieri and Serangium parcestosum (Iperti 1999). The discrepancy in species
number from these different sources can not solely be accounted for by the addition
of new species arriving in Europe but is an indication of the dynamic state of coc-
cinellid taxonomy and the difficulty of establishing a checklist for Europe. Not only
is the taxonomy of coccinellids under review but also the arrival of new species is
ongoing; recently the UK Ladybird Survey (www.ladybird-survey.org) reported the
first British record of Cynegetis impunctata (Thomas et al. 2009). There is also con-
siderable variation in reported coccinellid diversity between countries. Great Britain
is relatively species poor with only 46 species (Majerus et al. 2006b) whereas in
contrast the Netherlands have 86 native coccinellid species. The proportion of alien
species for this group is quite high in Europe, with 13 species observed in the wild
to date. Two of these are native to Europe but alien within Great Britain (Henosepil-
achna argus, Scymnus impexus) and Sweden (Scymnus impexus). For the remainder of
this section only the 11 species alien to Europe (and not the three alien species in
Europe) will be considered.
The majority of coccinellid species (about 90 %) are beneficial predators (others
are phytophagous or mycophagous); consequently coccinellids have played a signifi-
cant role in the development of biological control strategies (Berthiaume et al. 2007,
Brown and Miller 1998, Galecka 1991, Gurney and Hussey 1970, Iperti 1999, Obry-
cki and Kring 1998). This has been a major factor in the movement of coccinellids
between countries worldwide.

8.4.2 Taxonomy of the coccinellid species alien to Europe

The family Coccinellidae belongs to the coleopteran superfamily Cucujoidea and is
a member of the phylogenetic branch of Coleoptera termed the Cerylonid complex
of families (Cerylonidae, Discolomidae, Alexiidae, Corylophidae, Endomychidae and
Lathridiidae). Worldwide there are six subfamilies of Coccinellidae: Sticholotidinae,
Chilocorinae, Scymninae, Coccidulinae, Coccinellinae and Epilachninae although a
recent phylogeny suggests a seventh subfamily, Ortaliinae (Fürsch 1990, Kovář 1996).
European species are mainly represented by three subfamilies: Scyminae, Chilocorinae
and Coccinellinae. There are very few European Sticholotinae, very few Coccidulinae
and only three species of Epilachninae (Iperti 1999). Although the species list for Coc-
cinellidae in Fauna Europaea (Audisio and Canepari 2009) includes representatives
from all six subfamilies.
Species alien to Europe are quite evenly represented between five of the six sub-
families. Three species are observed in the subfamily Coccidulinae (two Coccidulini
 Ladybeetles (Coccinellidae). Chapter 8.4 295

and one Noviini) and in the Scymninae (two Scymnini and one Hyperaspidini). Two
species are in the Chilocorinae (two Chilocorini) and Coccinellinae (two Coccinel-
lini). One species is in the Sticholotidinae (Sticholotidini). There are no Epilachninae
that are alien to Europe (although Henosepilachna argus is alien in Europe).
Most species in the Epilachninae are phytophagous, while the majority of spe-
cies in the other subfamilies are predatory. The preferred diets of the two feeding
stages in the life-cycle, the larval and adult stages, are generally the same. Most
predatory ladybirds feed on either aphids or coccids (a few feed on both), however
some predatory species feed on mites, adelgids, aleyrodids, ants, chrysomelid larvae,
cicadellids, pentatomids, phylloxera, mycophagous coccinellids and psyllids (Dixon
2000). Indeed, a small number of species within the Coccinellinae and Epilachninae
are mycophagous, feeding on the hyphae and spores of fungi. There is also consider-
able variability in the degree of dietary specialisation between species (Hodek 1996).
Some species have a very narrow preferred prey range, such as a single species of
mite, aphids of a single genus, or plants of a single family, other species have a wide
prey range. Harmonia axyridis, for example, will feed on aphids, coccids, adelgids,
psyllids, and the eggs and larvae of many other insects, including other coccinellids
and lepidopterans (Legaspi et al. 2008, Ware and Majerus 2008). Ladybirds exhibit
complex adaptations to specific or more general diets such as mandibular dentition,
gut length and structure, and morphological features that affect mobility (Hodek
1996). Many predatory coccinellids will feed on alternative foods, such as pollen,
nectar, honey-dew and fungi (many also resort to cannibalism) when preferred prey
are scarce (De Clercq et al. 2005, Hodek 1996).
Coccinellids are distinguished from the remainder of the Cerylonid complex of
families by a number of adult characteristics: five pairs of abdominal spiracles, tento-
rial bridge is absent, anterior tentorial branches are separated, frontoclypeal suture
absent, apical segment of maxillary palpus never aciculate, galea and lacinia separated,
mandible with reduced mola, front coxal cavities open posteriorly, middle coxal cavi-
ties open outwardly, metaepimeron parallel-sided, femoral lines present on abdominal
sternite 2, tarsal formula 4-4-4 or 3-3-3, tarsal segment 2 usually strongly dilated be-
low (Kovář 1996). In Europe, the diagnostic features of the family Coccinellidae can
be considered in more simple terms (Majerus 2004). They are small to medium sized
beetles (1.3–10 mm in length). There body shape is oval, oblong oval or hemispherical
(upper surface convex and lower surface flat). They have large, compound eyes. The
antennae are often 11-segmented but this figure varies and can be as low as seven. The
mouthparts consist of large, strong mandibles; four-segmented maxillary palps (termi-
nal segment axe shaped) behind the mandibles; labium divided into the pre-labium
and post-labium; three-segmented labial palps; and the labrum. The head can be partly
withdrawn under the pronotum. The pronotum is broader than long and has anterior
extensions at the margin. The legs are short and can be retracted into depressions under
the body. The tarsi are usually four segmented but the third segment is small and hid-
den in the end of the second segment. Each tarsus bears two claws. The abdomen has
ten segments (Kovář 1996, Majerus et al. 2006a).
296 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

8.4.3 Temporal trends of introduction in Europe of alien coccinellids

The first species of coccinellid to be introduced into Europe was the vedalia beetle, R.
cardinalis, for the control of the cottony cushion scale (coccid), Icerya purchasi (Figure
8.4.1). Two further species were introduced during the early twentieth century (mainly
to the Mediterranean regions including France, Portugal and Italy) but there then fol-
lowed a period of stagnation and respect to biological control in general. This correlates
with the trend towards chemical insect pest control with the development of synthetic
pesticides. From the 1980’s onwards there were a considerable number of introduc-
tions on an extensive scale across Europe through the use of tropical coccinellids to
control glasshouse pest insects.

8.4.4 Biogeography of the coccinellid species alien to Europe

Each continent has a specific fauna of coccinellidae. Belicek (1976) stated that “many
species develop their cycles in life zones delineated by the general physiography of the
continents (mountainous barriers) and climatic patterns combined with the types of
vegetation in a given zone”. Glaciation had profound effects on the distribution of coc-
cinellids and the level of endemism is further controlled by ecological factors including
temperature, food and natural enemies.
The temperate zones of Europe and North America are heavily infested by Aphi-
dae and grasslands in these regions contain coccinellids from the tribus Coccinellini
(Coccinella spp., Adalia spp., Harmonia spp.) and Hippodamiini, Cheilomenini and
Scymnini. Open deciduous and coniferous forests in this temperate zone contain other
genera of Coccinellini (Anatis spp., Myrrha spp., Myzia spp.). Tropical zones in central
and South Africa, South America, India and China where Coccidae are abundant are
characterised by coccinellids from the tribus Chilocorini (Chilocorus spp., Exochomus
spp., Brumus spp.), Scymnini, Hyperaspini, Coccidulini and Noviini. In the Mediter-
ranean regions of Europe, aphids and coccids are found together and are attacked by
coccinellids from the temperate and tropical zones (Iperti 1999).
It is interesting to note that coccinellids native to temperate zones enter either sim-
ple quiescence or intense diapause as adults. In contrast, exotic species such as Rhyzo-
bius lophanthae and Cryptolaemus montrouzieri do not enter quiescence or diapause but
instead resist drastic changes in climate by reducing the speed of development during
winter but not entirely stopping it (Iperti 1999).
The early introductions of alien coccinellids were characteristically as classical bio-
logical control agents; the predatory coccinellid originated from the same country as
the target pest insect. So, for example, both R. cardinalis and I. purchasi originated from
Australia; R. lophanate and various Diaspididae (Pseudolacaspis pentagona, Quadraspidi-
otus perniciosus, Chrysomphalus dictyospermi, Parlatoria blanchardi) from Australia and
New Zealand; C. montrouzieri and Planococcus citri from Australia. Notably all these
species are from tropical regions and were introduced into Mediterranean regions for
 Ladybeetles (Coccinellidae). Chapter 8.4 297

Figure 8.4.1. Temporal trends in the mean number of new records per year of coccinellid species alien to
Europe from 1875 to 2008. The number above the bar indicates the total number of alien species newly
recorded during the considered time period.

control purposes (Figures 8.4.1 and 8.4.2). In contrast, the coccinellid species selected
to reinforce the activity of native natural enemies in temperate regions of Europe are
from temperate regions of the globe for example, temperate Asia (H. axyridis) or North
America (Hippodamia convergens).

8.4.5 Distribution of alien Coccinellids in Europe

The distribution of alien coccinellids in Europe mirrors the biogeographical distribu-
tion and patterns of introduction (Figure 8.4.3). Some species have dispersed widely;
H. axyridis has spread rapidly from countries where it was deliberately introduced to
many others across Europe. Furthermore, the commercial production of coccinellids
by biological control companies and local producers led to a rapid increase in distribu-
tion thoughout the 1990’s.

8.4.6 Use of alien coccinellids for biological control in Europe

The ecosystem service that predatory coccinellids provide in consuming pest insects
has been recognised for over a century. The vedalia ladybird, R. cardinalis, is consid-
ered to have initiated modern biological pest control. It was released as a classical bio-
298 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

Figure 8.4.2. Origin of the 11 alien coccinellid species established in Europe.

logical control agent (native to Australia) in 1887 to control an alien cottony cushion
scale (coccid), I. purchasi, which was threatening the citrus industry of California. The
vedalia ladybird and the cottony cushion scale are still present in Californian citrus
groves but the ecological balance between predator and prey ensures that the pest is no
longer a problem (Caltagirone 1989, Majerus et al. 2006a).
The successful introduction of R. cardinalis for the control of I. purchasi result-
ed in considerable focus on Coccinellidae for importation programmes worldwide
(Obrycki and Kring 1998). Over 40 species of coccinellid were introduced to North
America following R. cardinalis during a period colloquially referred to as the “la-
dybird fantasy” (Caltagirone 1989, Dixon 2000). This worldwide phenomenon was
mainly ineffectual; only four of over 40 species introduced to North America during
this time established (Caltagirone 1989). In recent times there have been 155 at-
tempts to control aphids and 613 to control coccids worldwide through the introduc-
tion of ladybirds (Dixon 2000). On a scale of success (complete, substantial, partial
or no control) only one attempt to control aphids using coccinellids has been ranked
as substantially successful and none have been completely successful (Dixon 2000).
In contrast, 23 complete and 30 substantial successes have been achieved against
coccids (Dixon 2000). In a few cases the introduced coccinellid species has had far-
reaching, unacceptable impacts on biodiversity and so has been deemed an invasive
species. Harmonia axyridis, harlequin ladybird, is the only such example in Europe
(Brown et al. 2008a).
All of the 11 alien coccinellids in Europe have been intentionally released as bio-
logical control agents of pest insects. The first coccinellid to be introduced to Europe
was R. cardinalis as a predator of I. purchasi in 1888 (Portugal), 1901 (Italy) and 1912
(Italy and France). This species was subsequently released through the mid and late
1900s to Italy, Portugal, Israel, France, Spain, Malta, Great Britain, Albania, Cyprus,
Switzerland and the Ukraine. Cryptolaemus montrouzieri, native to Australia, was in-
tentionally released to control mealybugs (Pseudococcidae), Planococcus citri, from
1908 in Italy. Subsequent releases were made in Spain (1926), Corsica (1970), France
 Ladybeetles (Coccinellidae). Chapter 8.4 299

Figure 8.4.3. Colonisation of European countries and islands by coccinellids alien to Europe where
known. Scale = total number of recorded alien coccinellids.

(1974), Portugal (1984) and Sweden (2001). This species is considered established
in all the countries where it has been released other than Sweden (for which the sta-
tus of this species is unknown). Cryptolaemus montrouzieri has been used extensively
through augmentation (release of reared adults) and was the first coccinellid used to
demonstrate an inoculative approach (whereby the aim is introduce a small number of
individuals into a crop system with the expectation that they will reproduce and their
offspring will continue to provide control of the target pest for an extended period of
time). Cryptolaemus montrouzieri is easy and cheap to culture on mealybugs (Majerus
2004). Rhyzobius lophanthae is a species native to New Zealand which was introduced
to Italy in 1908 for the control of Diaspididae (armoured scale insects). It has been
released widely in European countries including: Portugal (1930 and 1984), Spain
(1958), Sardinia (1973), France (1975), Greece (1977) and Germany (2000). This
species has recently been reported as established in London, Great Britain (Natural
History Museum, 2008).
300 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

Figure 8.4.4. Harlequin ladybeetle (Harmonia axyridis). Credit: Mark Bond

8.4.6.1 Control of Scale Insects

A number of coccinellid species have been used in historically significant and success-
ful projects for the biological control of scale (Borges et al. 2006, Erler 2001, Katsoy-
annos 1997) including R. cardinalis and R. lophanthae. Other species introduced to
Europe for control of scales include Rhyzobius forestieri, Nephus reunioni, Chilocorus
nigritus and Chilocorus kuwanae.
Rhyzobius forestieri (native to Australia) has established in Italy, France, Greece and
Albania. In the Cambos coastal plain of Greece this species is now considered the most
abundant species of coccinellid within the coccidophagous guild (Katsoyannos 1997).
Nephus reunioni (native to Africa) was intentionally released in a number of countries
(Italy, Portugal, France, Greece, Albania and Spain) and is now considered to be estab-
lished in Italy and Portugal. Chilocorus nigritus is native to the Indian sub-continent
and South East Asia and is a candidate biological control agent for the control of spe-
cies within the Coccoidea including three economically important families (Diaspidi-
dae, Pseudococcidae and Coccidae). It has a recent history, 1985 onwards, of introduc-
tion to a number of countries: Italy, Denmark, France, Germany, Netherlands, Great
Britain and Albania. Chilocorus kuwanae is a biological control agent of scale insects
and was introduced to Europe (Albania and Italy) from Asia in 1989.

8.4.6.2 Control of Aleyrodidae

The family Aleyrodidae comprises the commonly referred to whiteflies. Over fifty
species of coccinellidae attack eggs and immature stages of whitefly pests (Obrycki
and Kring 1998, Yigit et al. 2003). There is interesting variation in the preda-
 Ladybeetles (Coccinellidae). Chapter 8.4 301

Figure 8.4.5. Adults of Cynegetis impunctata. Credit: Gilles San Martin

tory behaviour of these polyphagous coccinellids; some are mobile, seeking out
prey, and others are sedentary, and complete preimaginal development on one leaf
(Obrycki and Kring 1998). In Europe one species, Serangium parcesetosum, has been
introduced for the control of whitefly (Bemisia tabaci). Serangium parcesetosum was
introduced from its native range of Asia and the Indian subcontinent to France
including Corsica (Majka and McCorquodale 2006). A further species Delphastus
catalinae, native to North America, has been introduced in glasshouses within Al-
bania and Russia for the control of Bemisia tabaci and Trialeurodes vaporariorum
(Kutuk and Yigit 2007, Legaspi et al. 2008). However, this species has not estab-
lished in the wild. Studies on the thermal biology of D. catalinae, assessing the ef-
fects of temperature on development, voltinism and survival in the laboratory and
field (non-indigenous range), indicate a strong correlation between survival in the
laboratory at 5 ºC and in the field in winter (Simmons and Legaspi 2004, Simmons
and Legaspi 2007). Delphastus catalinae died out quickly in winter temperatures
and this suggests that the probability of establishment is low in regions that experi-
ence low temperatures and scarcity of suitable food for part of the year (van Len-
terenet et al. 2003). In the absence of studies on cold tolerance it is insufficient to
assume that, on the basis of climate matching, winter would be an effective barrier
to establishment of species originating from warmer climatic zones (van Lenteren et
al. 2006). Risk assessments should also be sufficiently detailed to encompass strain
specific parameters; the release of a non-diapausing strain versus a diapausing strain
could result in very different impacts (van Lenteren et al. 2006). Furthermore, im-
pacts through consumption of non-target hosts and dispersal require considerable
attention (van Lenterenet et al. 2003). So, for example, although D. catalinae is not
anticipated to survive winter temperatures in northern Europe, it is oligophagous
302 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

Figure 8.4.6. Adult of the phytophagous bryony ladybeetle, Henosepilachna argus. Credit: Mike Maje-
rus.

and reported as an intra-guild predator of the aphelinid parasitoid Encarsia sophia

(Zang and Liu 2007).

8.4.6.3 Control of Aphids

Hippodamia convergens and H. axyridis have both been released extensively through-
out Europe for the control of aphids. Hippodamia convergens is native to America and
several billion are collected annually from overwintering sites in California and sold
throughout America. This practice has been shown to be highly ineffective because of
adult dispersal (Dixon 2000, Roy and Majerus, unpubl.). Furthermore, removal of H.
convergens is considered to have adverse effects on local populations and, in America,
is responsible for the distribution of two ladybird parasites (the braconid wasp, Dino-
campus coccinellae and the microsporidian, Nosema hippodamiae) (Saito and Bjornson
2006) and vectoring of plant pathogens (dogwood anthracnose fungus) (Bjornson
2008). This coccinellid has been released in Belgium, Sweden, Denmark, Albania and
the Czech Republic in the 1990s and early 2000. It is unknown whether or not it is
established.
The use of H. axyridis as an augmentative biological control agent (mass reared
and released) has been widespread (Berkvens et al. 2008, Brown et al. 2008a). In 1982
it was introduced into France and has since been reared continuously over 100 gen-
erations on industrially produced eggs of the moth, Ephestia kuehniella (Brown et al.
2008a). It has since been introduced to a number of countries across Europe and also
spread to others which had not intentionally released it (Table 8.4.3).
 Ladybeetles (Coccinellidae). Chapter 8.4 303

Figure 8.4.7. Larva of Henosepilachna argus. Credit: Gilles San Martin

8.4.7 Ecosystems and habitats invaded in Europe by alien Coccinellids

Coccinellid species can be classified as stenotopic or eurytopic (Hodek 1993, Iperti

1991). Microclimate is considered to be a particularly important feature of a coc-
cinellid habitat. Many species of ladybird exhibit a preference for specific vegetation
types or certain strata of the habitat. Coupled with this is the requirement for suitable
food in sufficient abundance. Habitat preference varies seasonally as the microclimatic
characteristics of a habitat change, which in turn influences the distribution of prey
populations and the behaviour of coccinellids. Iperti (1999) documents the succession
of aphid outbreaks in south eastern France; during a normal year aphids first appear on
low plants and shrubs, they then progress to cultivated low plants and early deciduous
trees and develop on cultivated trees and shrubs. However, climatic conditions vary
annually and so it is difficult to predict the behaviour of coccinellids, particularly in a
period of climate change.
There is a strong trend for alien coccinellids to occur in urban or cultivated habitats
in Europe. Almost all species are most prevalent in recently cultivated agricultural, hor-
ticultural and domestic habitats, gardens and parks and greenhouses (EUNIS catego-
ries I I1, I2, J100; see appendix II). Harmonia axyridis, the most invasive of the alien
coccinellids in Europe, follows this pattern although there have been a considerable
number of records in Great Britain from natural habitats (Brown et al. 2008b). Indeed,
H. axyridis is documented from both woodlands and forest habitats, small anthropo-
genic woodlands, parks and gardens, agricultural and horticultural habitats as well as
from buildings in cities, towns and villages.
The abundance of native and alien coccinellid species in urban habitats and their
tendency to aggregate in large numbers during autumn and winter enhances their
304 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

visibility to people. This aggregation behaviour can be exploited by biological control

practitioners through the collection and release of large numbers of beetles but species
that exhibit this behaviour, such as H. axyridis, are increasingly seen as nuisance insects
in domestic dwellings (Roy and Majerus 2006, Roy et al. 2008).

8.4.8 Ecological and economic impacts of alien coccinellids

The ecological and economic impacts of alien coccinellids are not well documented.
Many authors have noted the low success rate of coccinellids as biological control
agents of aphids (Dixon 2000, Iperti 1999, Majerus et al. 2006a). The success of coc-
cinellids as biological control agents of coccids is higher than that of aphids but still
relatively low at only 40 % of cases studied being designated as exerting complete or
substantial control (Iperti 1999).
Rodolia cardinalis has been heralded as a success story for biological control (Calta-
girone 1989). This species has been introduced into 33 countries to control I. purchasi
and has yielded complete control in 26 countries (North America, Argentina, Peru,
Chile, Portugal, Uruguay, Venezuela, France, Italy, Spain, Greece, Morocco, Tunisia,
Turkey, Egypt, India, Japan and New Zealand); substantial control in four countries
(Russia, Libya, the Bahamas, Ecuador) and partial control in two countries (Seychelles
and Mauritius). A similar rate of success was achieved through the acclimatization of
C. montrouzieri to control Pseudococcus spp. (Iperti 1999). Therefore, R. cardinalis and
C. montrouzieri have contributed economic benefits through the ecosystem service
they provide. Indeed, the initial cost of the R. cardinalis introduction programme in
California 1888 was $1 500 with a return in just over a year of millions of dollars
(Majerus 2004).
The lack of success of aphidophagous coccinellids has been attributed to asyn-
chrony between the reproductive and development rates of the predatory coccinellids
and their aphid prey (Dixon 2000). Furthermore, many aphidophagous coccinellids,
in temperate climates, are univoltine whereas aphids are multivoltine. Coccidophagous
coccinellids tend to stay in a localised area throughout their life cycle and, in contrast,
aphidophagous coccinellids disperse widely (Iperti 1999).
Most intentional insect introductions do not cause ecological or economic prob-
lems, indeed of all the intentionally introduced insects to North America only 1.4 %
have caused problems (van Lenteren et al. 2003). Indeed insect introductions are
considered to be relatively safe: less than 1 % cause a population level effect in non-
targets and only 3–5 % may have caused smaller scale effects (van Lenterenet et al.
2003). However, a number of coccinellids are documented as having non-target ef-
fects (van Lenterenet et al. 2003). Cryptolaemus montrouzieri is reported to lower the
effectiveness of an introduced natural enemy (Dactylopius opuntiae) for weed control
(Goeden and Louda 1976). The most infamous coccinellid introduction is undoubt-
edly H. axyridis (Majerus et al. 2006b, Roy and Majerus 2006, Roy et al. 2005, Roy
and Wajnberg 2008).
 Ladybeetles (Coccinellidae). Chapter 8.4 305

Harmonia axyridis has been released as a classical biological control agent in North
America since 1916. It has been commercially available in Europe since the 1980s and has
many attributes that contribute to its economic viability, including its polyphagous nature.
Harmonia axyridis preys on a wide variety of tree-dwelling homopteran insects, such as
aphids, psyllids, coccids, adelgids and other insects (Koch et al. 2006). In North America,
as well as offering effective control of target pests, such as aphids in pecans (Tedders and
Schaefer 1994), H. axyridis is also providing control of pests in other systems such as Aphis
spiraecola in apple orchards (Brown and Miller 1998) and several citrus pests (Michaud
2002). In both Asia and North America, H. axyridis has been reported to contribute to
control of aphids on sweet corn, alfalfa, cotton, tobacco, winter wheat and soybean (Longo
et al. 1994). The spread and increase of H. axyridis throughout Europe could, therefore,
prove to be beneficial to ecosystem services through the reduction in aphid numbers below
economically damaging levels and subsequent reduction in the use of chemical pesticides.
The polyphagous nature of H. axyridis means that negative impacts on non-target
prey species would appear to be inevitable (Majerus 2006, Pell et al. 2008). However,
there is very limited empirical evidence on this subject and studies considering the
effects of H. axyridis on the population demography of non-target aphids, coccids
and other prey species away from crop systems have not been conducted. Harmonia
axyridis has been implicated as a potential predator of immature monarch butterflies,
Danaus plexippus, an aposematic species that contains defensive chemicals (Koch et al.
2003). Laboratory studies have also indicated the potential for H. axyridis to engage
in intra-guild predation (Pell et al. 2008, Roy et al. 2008, Ware and Majerus 2008).
It is likely that many other species will be directly or indirectly affected by the arrival
of H. axyridis. Indeed, intraguild predation is thought to be an important force in
structuring aphidophagous ladybird guilds (Yasuda et al. 2004) and so H. axyridis has
the potential to dramatically disrupt native guilds in Europe. Harmonia axyridis is a
large, aggressive, polyphagous coccinellid (with a tendency for intraguild predation)
that could impact on the abundance of native coccinellids and reduce their available
niches (Legaspi et al. 2008).
The wide dietary range of H. axyridis coupled with its ability to disperse rapidly,
forage widely and continuously breed gives this species the potential to significantly
reduce European populations of coccids and aphids. This is, of course, considered ben-
eficial in crop and horticultural systems, but not in other habitats where such direct
competition for prey may result in a reduction in biodiversity and declines in native
beneficial predators and parasitoids of aphids and coccids (Majerus 2006).
Majerus et al. (2008) noted that the negative effects of H. axyridis on other aphido-
phages are likely to be the result of a complex range of interactions, with H. axyridis in
general having a competitive edge through resource competition, intraguild predation
and a more plastic phenotype. A more rapid development rate, continual breeding
ability and lack of diapause requirement, efficient chemical defence and relatively large
size would provide H. axyridis with a significant reproductive advantage over many
native British species. The pattern is anticipated to be widespread throughout Europe
(Brown et al. 2008a).
306 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

8.4.10 Conclusions
Coccinellids have been introduced widely throughout Europe for the biological con-
trol of pest insects. Some of these species have established and for others the status is
unknown. It is difficult to estimate the proportion of alien coccinellids in Europe for
two reasons: there is not a definitive European check list for coccinellids and the status
of some of the alien species is unknown. However, the proportion of alien coccinellids
appears to be higher (approximately 5–10 %) than the proportion of aliens for other
taxonomic groups (3.1 % alien Diptera). Only one species (H. axyridis) is considered
to be invasive.

Acknowledgements
HER is based in the Biological Records Centre (within the NERC Centre for Ecology
& Hydrology) and receives co-funding from the Joint Nature Conservation Com-
mittee and the Natural Environment Research Council. AM is funded by the Institut
National de la Recherche Agronomique (INRA). The authors gratefully acknowledge
Stephanie Ames for production of the European distribution map. Michael E.N. Ma-
jerus and Peter M.J. Brown are thanked for insightful discussions on the European
species check list.

References
Adriaens T, Branquart E, Maes D (2003) The Multicoloured Asian Ladybird Harmonia axyridis
Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belgian
Journal of Zoology 133: 195–196.
Adriaens T, San Martin y Gomez G, Maes D (2008) Invasion history, habitat preferences and
phenology of the invasive ladybird Harmonia axyridis in Belgium. Biocontrol 53: 69–88.
Audisio P, Canepari C (2009) Fauna Europaea - Coccinellidae. http://www.faunaeur.org/full_
results.php?id=11062.
Belicek J (1976) Coccinellidae of Western Canada and Alaska with analyses of the transmon-
tane zoogeographic relationship between the fauna of british Columbia and Alberta. Ques-
tiones Entomology: 283–409.
Berkvens N, Bonte J, Berkvens D, Tirry L, De Clercq P (2008) Pollen as an alternative food for
Harmonia axyridis. Biocontrol 53: 201–210.
Berthiaume R, Hébert C, Cloutier C (2007) Comparative use of Mindarus abietinus (Homop-
tera: Aphididae) by two coccinellids (Coleoptera: Coccinellidae), the native Anatis mali
and the exotic Harmonia axyridis, in a Christmas tree plantation. Environmental Entomol-
ogy 36: 319–328.
 Ladybeetles (Coccinellidae). Chapter 8.4 307

Bjornson S (2008) Natural enemies of the convergent lady beetle, Hippodamia convergens Guer-
in-Meneville: Their inadvertent importation and potential significance for augmentative
biological control. Biological Control 44: 305–311.
Booth RG (1998) A review of the species resembling Chilocorus nigrita (Coleoptera: Coccinelli-
dae): potential agents for biological control. Bulletin of Entomological Research 88: 361–367.
Booth RG, Cross AE, Fowler SV, Shaw RH (1995) The biology and taxonomy of Hyperaspis
pantherina (Coleoptera: Coccinellidae) and the classical biological control of its prey, Or-
thezia insignis (Homoptera: Ortheziidae). Bulletin of Entomological Research 85: 307–314.
Borges I, Soares AO, Hemptinne JL (2006) Abundance and spatial distribution of aphids and
scales select for different life histories in their ladybird beetle predators. Journal of Applied
Entomology 130: 356–359.
Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Vir-
ginia and the impact of invasion by Harmonia axyridis. Entomological News 109: 143–151.
Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hagg T, Kenis M, Klausnitzer
BEM, Kovář I, Loomans AJ, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE,
Ternois V, Zakharov I, Roy DB (2008a) Harmonia axyridis in Europe: spread and distribu-
tion of a non-native coccinellid. Biocontrol 53: 5–21.
Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2008b) Harmonia ax-
yridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid.
Biocontrol 53: 55–67.
Caltagirone L E (1989) The history of the vedalia beetle importation to California and its
impact on the development of biological control. Annual Review of Entomology 34: 1–16.
De Clercq P, Bonte M, Van Speybroeck K, Bolckmans K, Deforce K (2005) Development and
reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehn-
iella (Lepidoptera: Phycitidae) and pollen. Pest Management Science 61: 1129–1132.
Dixon A FG (2000) Insect predator-prey dynamics: Ladybeetles and Biological Control. Cam-
bridge: Cambridge University Press. 257 pp.
Erler F, Tunc I (2001) A survey (1992–1996) of natural enemies of Diaspididae species in An-
talya, Turkey. Phytoparasitica 29: 299–305.
Fowler S V (2004) Biological control of an exotic scale, Orthezia insignis Browne (Homoptera:
Ortheziidae), saves the endemic gumwood tree, Commidendrum robustum (Roxb.) DC.
(Asteraceae) on the island of St. Helena. Biological Control 29: 367–374.
Frank J H, McCoy ED (2007) The risk of classical biological control in Florida. Biological
Control 41: 151–174.
Fürsch H (1990) Taxonomy of coccinellids, corrected version. Coccinella 2: 4–6.
Galecka B (1991) Distribution and role of coccinellids in an agricultural landscape. In: Polgar
L, Chambers RJ, Dixon AFG, Hodek I (Eds) Behaviour and Impact of Aphidophaga. The
Hague : SPB Academic Publishing, 137–141.
Goeden RD, Louda SM (1976) Biotic interference with insects imported for weed control.
Annual Review of Entomology 21: 325–342.
Gurney B, Hussey NW (1970) Evaluation of some coccinellid species for biological control of
aphids in protected cropping. Annals of Applied Biology 65: 451–458.
308 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

Hamid HA, Michelakis S (1994) The importance of Cryptolaemus montrouzieri Mulsant (Col.:
Coccinellidae) in the control of the citrus mealy bug Planococcus citri (Risso) (Hom.: Coc-
coidea) under specific conditions. Journal of Applied Entomology-Zeitschrift Fur Angewandte
Entomologie 118: 17–22.
Hill M, Baker R, Broad G, Chandler PJ, Copp GH, Ellis J, Jones D, Hoyland C, Laing I, Long-
shaw M, Moore N, Parrott D, Pearman D, Preston C, Smith RM, Waters R (2005) Audit
of non-native species in England. Peterborough, UK: English Nature. 82 pp.
Hodek I (1993) Habitat and food specificity in aphidophagous predators. Biocontrol Science
and Technology 3: 91–100.
Hodek I (1996) Food Relationships. In: Hodek I, Honek A (Eds) Ecology of Coccinellidae. The
Hague: Kluwer Academic Publishers, 143–238.
Humble LM (1994) Recovery of additional exotic predators of balsam woolly adelgid, Adelges
piceae (Ratzeburg) (Homoptera, Adelgidae), in British Columbia. Canadian Entomologist
126: 1101–1103.
Iperti G (1991) Abiotic and biotic factors influencing the distribution of the aphidophagous
coccinellidae. In: Polgar L, Chambers RJ, Dixon AFG, Hodek I (Eds) Behaviour and Im-
pact of Aphidophaga. The Hague: SPB Academic Publishing, 163–166.
Iperti G (1999) Biodiversity of predaceous coccinellidae in relation to bioindication and eco-
nomic importance. Agriculture Ecosystems & Environment 74: 323–342.
Izhevsky SS, Orlinsky AD (1988) Life history of the importaed Scymnus (Nephus) reunioni
(Col.: Coccinellidae) predator of mealybugs. Entomophaga 33: 101–114.
Katsoyannos P (1997) Status and importance of Rhyzobius forestieri (Col.: Coccinellidae) on
citrus at Chios island, Greece, nine years after its introduction. Entomophaga 42: 387–392.
Koch RL, Hutchison WD, Venette RC, Heimpel GE (2003) Susceptibility of immature mon-
arch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by
Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control 28: 265–270.
Koch RL, Venette RC, Hutchison WD (2006) Invasions by Harmonia axyridis (Pallas) (Cole-
optera: Coccinellidae) in the Western Hemisphere: Implications for South America. Neo-
tropical Entomology 35: 421–434.
Kovář I (1996). Phylogeny. In: Hodek I, Honek A (Eds) Ecology of Coccinellidae. The Hague:
Kluwer Academic Publishers, 19–32.
Kutuk H, Yigit A (2007) Life table of Delphastus catalinae (Horn) (Coleoptera: Coccinellidae)
on cotton whitefly, Bemisla tabaci (Genn.) (Homoptera: Aleyrodidae) as prey. Journal of
Plant Diseases and Protection 114: 20–25.
Legaspi JC, Legaspi BC, Simmons AM, Soumare M (2008) Life table analysis for immatures
and female adults of the predatory beetle, Delphastus catalinae, feeding on whiteflies under
three constant temperatures. Journal of Insect Science 8: 07.
Longo S, Mazzeo G, Russo A, Siscaro G (1994) Aonidiella citrina (Coquillet) a new pest of
citrus in Italy. Informatore Fitopatologico 44: 19–25.
Majerus M, Strawson V, Roy HE (2006a) The potential impacts of the arrival of the harlequin
ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecological En-
tomology 31: 207–215.
Majerus MEN (1994). Ladybirds. Somerset: Harper Collins Publisher.
 Ladybeetles (Coccinellidae). Chapter 8.4 309

Majerus MEN (2006a) The impact of male-killing bacteria on the evolution of aphidophagous
coccinellids. European Journal of Entomology 103: 1–7.
Majerus MEN, Roy HE, Brown PMJ, Ware RL (2006b) Guide to Ladybirds of the British Isles.
Shrewsbury: Field Studies Council.
Majka CG, McCorquodale DB (2006) The Coccinellidae (Coleoptera) of the Maritime Prov-
inces of Canada: new records, biogeographic notes, and conservation concerns. Zootaxa
1154: 49–68.
Malausa JC, Franco E, Brun P (1988) Establishment on the Cote-Dazur and in Corsica of
Serangium parcesetosum (Col.: Coccinellidae), a predator of the citrus whitefly, Dialeurodes
citri (Hom.: Aleyrodidae). Entomophaga 33: 517–519.
Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera:
Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea.
Environmental Entomology 31: 827–835.
Obrycki JJ, Kring TJ (1998) Predaceous Coccinellidae in biological control. Annual Review of
Entomology 43: 295–321.
Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving
Harmonia axyridis: a review of current knowledge and future perspectives. Biocontrol 53:
147–168.
Phoofolo MW, Giles KL, Elliott NC (2008) Larval life history responses to food deprivation
in three species of predatory lady beetles (Coleoptera: Coccinellidae). Environmental Ento-
mology 37: 315–322.
Ponsonby DJ, Copland MJW (2007a) Aspects of prey relations in the coccidophagous ladybird
Chilocorus nigritus relevant to its use as a biological control agent of scale insects in temper-
ate glasshouses. Biocontrol 52, 629–640.
Ponsonby DJ, Copland MJW (2007b) Influence of host density and population structure on
egg production in the coccidophagous ladybird, Chilocorus nigritus F. (Coleoptera: Coc-
cinellidae). Agricultural and Forest Entomology 9: 287–296.
Ricci C, Primavera A, Negri V (2006) Effects of low temperatures on Chilocorus kuwanae (Co-
leoptera: Coccinellidae) trophic activity. European Journal of Entomology 103: 547–551.
Roy HE, Majerus MEN (in press). Coccinellids in a Changing World. In Kindlmann P (Ed.)
Aphids in the changing world: Patterns and processes. Dordrecht, The Netherlands: Kluwer
Academic Publishers.
Roy HE, Majerus MEN (2006) Harmonia axyridis: A successful biocontrol agent or an invasive
threat? In: Eilenberg J, Hokkanen HMT (Eds) An ecological and societal approach to biologi-
cal control. Dordrecht, The Netherlands: Kluwer Academic Publishers, 295–309.
Roy HE, Brown PMJ, Rowland F, Majerus MEN (2005) Ecology of Harmonia axyridis. British
Wildlife 16: 403–407.
Roy HE, Brown PMJ, Ware RL, Michie L-J, Beckmann B, Majerus MEN (2008) The harle-
quin ladybird marches on. British Wildlife 19: 182–186.
Roy HE, Wajnberg E (2008). From biological control to invasion: the ladybird Harmonia ax-
yridis as a model species. Biocontrol 53: 1–4.
310 Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)

Saito T, Bjornson S (2006) Horizontal transmission of a microsporidium from the convergent

lady beetle, Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), to three
coccinellid species of Nova Scotia. Biological Control 39: 427–433.
Simmons AM, Legaspi JC (2004) Survival and predation of Delphastus catalinae (Coleoptera:
Coceinellidae), a predator of whiteflies (Homoptera: Aleyrodidae), after exposure to a
range of constant temperatures. Environmental Entomology 33: 839–843.
Simmons AM, Legaspi JC (2007). Ability of Delphastus catalinae (Coleoptera: Coccinellidae),
a predator of whiteflies (Homoptera: Aleyrodidae), to survive mild winters. Journal of En-
tomological Science 42: 163–173.
Smith SF, Krischik VA (2000) Effects of biorational pesticides on four coccinellid species (Co-
leoptera: Coccinellidae) having potential as biological control agents in interior landscapes.
Journal of Economic Entomology 93: 732–736.
Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera:
Coccinellidae) in the south-eastern United States. Entomological News 105: 228–243.
Thomas RJ, Majerus MEN, Brown PMJ, Roy HE (2009) A first record of Cynegetis impunctata
(Coleoptera: Coccinellidae). British Journal of Entomology and Natural History 21
van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans A
JM, Menzler-Hokkanen I, van Rijn PCJ Thomas MB, Tommasini MG, Zeng QQ (2003).
Environmental risk assessment of exotic natural enemies used in inundative biological con-
trol. Biocontrol 48: 3–38.
van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Evaluating risks of
releasing exotic biological control agents of arthropod pests. Annual Review of Entomology
51: 609–634.
Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japa-
nese coccinellids by the invasive ladybird Harmonia axyridis. Biocontrol 53: 169–188.
Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T (2004) Asymmetric larval interactions
between introduced and indigenous ladybirds in North America. Oecologia 141: 722–731.
Yigit A, Canhilal R (2005) Establishment and dispersal of Serangium parcesetosum Sicard
(Coleoptera, Coccinellidae), a predatory beetle of citrus whitefly, Dialeurodes citri Ashm.
(Homoptera, Aleyrodidae) in the East Mediterranean region of Turkey. Zeitschrift Fur Pflan-
zenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 112: 268–275.
Yigit A, Canhilal R, Ekmekci U (2003). Seasonal population fluctuations of Serangium parcese-
tosum (Coleoptera: Coccinellidae), a predator of citrus whitefly, Dialeurodes citri (Homop-
tera: Aleyrodidae) in Turkey’s eastern Mediterranean citrus groves. Environmental Entomol-
ogy 32: 1105–1114.
Zang LS, Liu TX (2007) Intraguild interactions between an oligophagous predator, Delphas-
tus catalinae (Coleoptera: Coccinellidae), and a parasitoid, Encarsia sophia (Hymenoptera:
Aphelinidae), of Bemisia tabaci (Homoptera: Aleyrodidae). Biological Control 41: 142–150.
Table 8.4.1. List and main characteristics of the Coccinellidae species alien to Europe. Status: A Alien to Europe C cryptogenic species. Country codes abbrevia-
tions refer to ISO 3166 (see appendix I). Habitat abbreviations refer to EUNIS (see appendix II). Phylogeny after (2 0, 35). Last update 01/03/2010.
Subfamily Status Regime Native 1st record Invaded countries Habitat Hosts References
Species range in Europe
Coccidulinae
Rhyzobius forestieri A Parasitic/ Australasia 1982, IT AL, FR, GR, IT I Coccids (Scale Katsoyannos (1997)
(Mulsant, 1853) Predator insects)
Rhyzobius A Parasitic/ Australasia 1908, IT AL, DE, ES, ES-BAL, FR, FR- I, J100 Coccids Erler (2001)
lophanthae Predator COR, GB, GR,GR-CRE, IT, (Scale insects
(Blaisdell, 1892) IT-SAR, IT-SIC, IL, MT, PT, specifically
PT-AZO, PT-MAD, Diaspididae)

Rodolia cardinalis A Parasitic/ Australasia 1888, PT AL, CH, CY, DE, ES, ES-BAL, I, J100 Coccids (Scale Caltagirone (1989), Frank and
(Mulsant, 1850) Predator ES-CAN, FR, FR-COR, GB, GR, insects) McCoy (2007)
GR-CRE, IL, IT, IT-SAR, IT-SIC,
MT, PT, PT-AZO, PT-MAD, UA
Scymninae
Hyperaspis A Parasitic/ Africa 2002, PT- PT-MAD U Orthezia Booth et al. (1995), Fowler
pantherina Fürsch, Predator MAD insignis (Scale (2004)
1975 insect)
Cryptolaemus A Parasitic/ Australasia 1908, IT AL, ES, ES-CAN, FR, FR-COR, I, J100 Mealybugs Hamid and Michelakis (1994),
Ladybeetles (Coccinellidae). Chapter 8.4

montrouzieri Predator GR,GR-CRE, IL, IT, IT-SAR, Smith and Krischik (2000)
Mulsant, 1853 IT-SIC, PT, RU, SE,
Nephus reunioni A Parasitic/ Africa 1983, FR AL, ES, FR, GR, IT-SAR, PT I Coccids (Scale Izhevsky and Orlinsky (1988)
Fürsch, 1974 Predator insects)
Chilocorinae
Chilocorus kuwanae A Parasitic/ Asia 1989, IT AL, IT I Coccids (Scale Ponsonby and Copland
Silvestri, 1909 Predator insects) (2007b), Ricci et al. (2006)
Chilocorus nigritus A Parasitic/ Asia 1994, IT AL, ,IT I, J100 Coccids (Scale Booth (1998), Ponsonby and
(Fabricius, 1798) Predator insects) Copland (2007a), Ponsonby
and Copland (2007b)
311
Subfamily Status Regime Native 1st record Invaded countries Habitat Hosts References
312

Species range in Europe

Sticholotidinae
Serangium A Parasitic/ Asia 1986, FR- FR, FR-COR I Aleyrodidae Yigit and Canhilal (2005),
parcesetosum Sicard, Predator COR Yigit et al. (2003)
1929
Coccinellinae
Harmonia axyridis A Parasitic/ Asia 1991, BE AL, AT, BE, BG, BY, CH, CZ, I Polyphagous Adriaens et al. (2003), Adriaens
(Pallas, 1773) Predator DE, DK, ES, ES-CAN, FR, insect et al. (2008), Brown et al.
FR-COR, GB, GR, GR-CRE, predator
(2008a), Brown et al. (2008b),
GR-ION, GR-SEG, HU, IL, IT, particularly
IT-SIC, , LI, LU, NL, NO, PT, aphids and Koch et al. (2003), Majerus
RO, RU, SE, SK, UA coccids (1994), Roy et al. (2005), Roy
and Wajnberg (2008)
Hippodamia A Parasitic/ North 1992, CZ AL, BE, CZ, DK, SE FA, Aphids Bjornson (2008), Phoofolo et
convergens Guerin- Predator America J100 al. (2008), Saito and Bjornson
Meneville, 1842
(2006)
Helen Roy & Alain Migeon / BioRisk 4(1): 293–313 (2010)
 Ladybeetles (Coccinellidae). Chapter 8.4 313

Table 8.4.2. List and main characteristics of the Coccinellidae species alien within Europe. Country
codes abbreviations refer to ISO 3166 (see appendix I). Habitat abbreviations refer to EUNIS (see appen-
dix II). Phylogeny after Fürsch (1990), Koch et al. (2006). Last update 01/03/2010.
SubFamily Regime Native Invaded Habitat* Hosts References
Species range countries
Scymninae
Scymnus Parasitic/ West GB, SE G, I2 Dreyfusia Humble (1994),
impexus Predator Palearctic piceae on Majka and
Mulsant, 1850* spruce and fir
McCorquodale (2006)
Epilachninae
Henosepilachna Phyto- West GB E5, I2, White bryony Hill et al. (2005)
argus (Geoffroy, phagous Palearctic FA (Bryonia
1762)* dioica)

Table 8.4.3. Summary of release dates and records from wild populations of Harmonia axyridis across
Europe. Adapted from Brown et al. (2008a). Updated: 01/03/2010
Country Year of release Year of first record in the wild
(blank if not released)
Ukraine 1964 Unknown
Belarus 1968 Unknown
Portugal 1984
France 1982 1991
Greece 1994 1998
Germany 1997 1999
Belgium 1997 2001
Netherlands 1996 2002
Spain 1995 2003
Switzerland 1996 2004
Luxembourg 2004
England and Channel Isl. 2004
Italy 1990s 2006
Czech Republic 2003 2006
Austria 2006
Denmark 2000s 2006
Wales 2006
Norway 2006
Poland 2007
Liechtenstein 2007
Sweden 2007
Northern Ireland 2007
Scotland 2007
Serbia 2008
Slovakia 2008
Hungary 2008
Bulgaria 2009
Romania 2009